Protein Family Content Uncovers Lineage Relationships and Bacterial Pathway Maintenance Mechanisms in DPANN Archaea

Abstract

DPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 3,197 genomes including 569 newly reconstructed genomes. Protein family content clearly separates the final set of 390 DPANN genomes from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.

Size-Fractionated Microbiome Structure in Subarctic Rivers and a Coastal Plume Across DOC and Salinity Gradients

“…They have been reported as the dominant archaeal group in Swedish boreal lakes with higher DOM aromaticity (Juottonen et al, 2020), and in Greenland ponds and lakes characterized by higher organic and inorganic carbon and total nitrogen concentrations (Bomberg et al, 2019). Their small genome and limited metabolic capacities suggest a symbiotic or parasitic lifestyle (Castelle et al, 2015(Castelle et al, , 2021. In anoxic environments, they have a potential role in nitrogen and sulfur cycling, and a syntrophic relationship with methanogenic archaea has been suggested based on their high co-occurrence (Liu et al, 2018(Liu et al, , 2021.…”

Conserved and lineage-specific hypothetical proteins may have played a central role in the rise and diversification of major archaeal groups

“…We collected 2618 genomes spanning all the recognized phyla and superphyla of the Archaea domain from the NCBI genome database (Additional file 1 : Table S1). To enable our analyses, we augmented the relatively limited sampling of the DPANN by adding 569 newly available DPANN metagenome-assembled genomes (MAGs) from low oxygen marine ecosystems, an aquifer adjacent to the Colorado River, Rifle, Colorado, and from groundwater collected at the Genasci dairy farm, Modesto, California [ 22 , 23 ]. The 3197 genomes were clustered at ≥ 95% average nucleotide identity (ANI) to generate 1749 clusters.…”

Comparative genomic insights into the evolution of Halobacteria-associated “Candidatus Nanohaloarchaeota”

“…1, S4–S6). In fact, AB_1215_Bin_137 is a MAG obtained from one of the Guaymas Basin (Gulf of California) sediment samples (29). It is classified into the order “ Ca .…”

“…It is widely believed that “ Ca . Nanosalinaceae” members adopt the “salt-in” strategy to resist the high osmotic pressure of hypersaline environments (22, 24), while AB_1215_Bin_137 inhabiting deep-sea sediment (29) may not be obligate to adapt to the extreme osmotic pressure. During the evolution of the “salt-in” strategy, the isoelectric point profiles of the predicted proteome became acid-shifted (22, 24), because the negatively charged amino acids can maintain the stability and activity of proteins in the hypersaline conditions (33).…”